JXB Advance Access originally published online on August 4, 2008
Journal of Experimental Botany 2008 59(12):3229-3245; doi:10.1093/jxb/ern200
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REVIEW-ARTICLE |
Hormone- and light-regulated nucleocytoplasmic transport in plants: current status
1Department of Biological Sciences, Yonsei University, 234 Heungup-Myun, Wonju-Si, 220–710, Korea
2Department of Biological Science, Ewha Woman's University, Seoul, 120–750, Korea
3Department of Life Science, Chung-Ang University, 221 Heukseok-Dong, Dongjak-Gu, Seoul, 156–756, Korea
* To whom correspondence should be addressed. E-mail: soohwan{at}yonsei.ac.kr; skkimbio{at}cau.ac.kr
Received 6 June 2008; Revised 4 July 2008 Accepted 7 July 2008
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Abstract |
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Top
Abstract
IntroductionThe gene regulation mechanisms underlying hormone- and light-induced signal transduction in plants rely not only on post-translational modification and protein degradation, but also on selective inclusion and exclusion of proteins from the nucleus. For example, plant cells treated with light or hormones actively transport many signalling regulatory proteins, transcription factors, and even photoreceptors and hormone receptors into the nucleus, while actively excluding other proteins. The nuclear envelope (NE) is the physical and functional barrier that mediates this selective partitioning, and nuclear transport regulators transduce hormone- or light-initiated signalling pathways across the membrane to mediate nuclear activities. Recent reports revealed that mutating the proteins regulating nuclear transport through the pores, such as nucleoporins, alters the plant's response to a stimulus. In this review, recent works are introduced that have revealed the importance of regulated nucleocytoplasmic partitioning. These important findings deepen our understanding about how co-ordinated plant hormone and light signal transduction pathways facilitate communication between the cytoplasm and the nucleus. The roles of nucleoporin components within the nuclear pore complex (NPC) are also emphasized, as well as nuclear transport cargo, such as Ran/TC4 and its binding proteins (RanBPs), in this process. Recent findings concerning these proteins may provide a possible direction by which to characterize the regulatory potential of hormone- or light-triggered nuclear transport.
Key words: Abscisic acid, auxin, brassinosteroid, cryptochrome, gibberellin, nuclear pore complex, nucleocytoplasmic transport, nucleoporins, phytochrome, Ran cycle
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Introduction |
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The nucleus segregates transcriptional regulation from cytoplasmic translational events, and this structural characteristic allows eukaryotic organisms to conduct multi-tiered and highly sophisticated life processes. Besides spatially separating transcription and translation, the nuclear membrane also regulates nucleocytoplasmic shuttling of proteins and RNA, providing a critical means for the cell to control signal transduction, downstream gene expression, and cellular function (Xu and Massague, 2004).
The molecular and biochemical mechanisms of nucleocytoplasmic transport of proteins have been best characterized in mammals and yeasts. Proteins are targeted and transported into the nucleus in an energy-dependent and regulated manner, and they usually carry a signal, called the nuclear localization signal (NLS) that can be recognized by a nuclear transporting carrier, such as a karyopherin protein-like importin 
/transportin. Proteins tracking back and forth between the nucleus and the cytoplasm also often harbour a nuclear exporting signal, and they are excluded from the nucleus by the action of another karyopherin member such as CRM1/exportin.
Once recognized by the importin , importin β, together with the ras-related small G-protein Ran, docks the transporting cargo to the cytoplasmic side of the NPC. Delivery through the NPC bucket is achieved by relaying the cargo between RanGDP- and RanGTP-binding nucleoporins in the NPC. RanBP1 and Ran GTPase-activating proteins (RanGAPs) maintain the Ran around the cytoplasmic side of the NE in the GDP-bound state; concomitantly, the Ran nucleotide exchange factor RCC1 (regulator of chromosome condensation 1) inside the nucleus maintains the majority of nuclear Ran in the GTP-bound state. The resulting unequal distribution between cytoplasmic Ran-GDP and nuclear Ran-GDP gives directionality to the nuclear import/export process: while cytoplasmic importin β preferentially binds to Ran-GDP, the karyopherins inside the nucleus associate with RanGTP, releasing imported cargo and binding exported cargo. Ran itself also cycles between the nucleus and the cytoplasm: nuclear transport factor-2 (NTF-2) imports cytoplasmic Ran-GDP into the nucleus, where RCC1 converts it to Ran-GTP (Meier, 2007; Sorokin et al., 2007). Figure 1 provides simplified diagrams illustrating the predicted locations of plant nuclear porin components of the NPC, and describing the current models for nucleocytoplasmic trafficking regulated by the Ran cycle and transport cargos in animals and plants.
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Plant hormones exert many of their physiological roles by altering nuclear processes. Molecular, genetic, and biochemical analyses dissecting hormone signalling pathways have proven to be very useful; many of the regulatory components and their modes of action have been characterized intensively during recent years. In particular, advances in proteomic technology have made it feasible to systematically and quantitatively analyse the molecular events of protein accumulation and post-translational modification. Proteomic approaches specifically designed to separate and contrast nuclear and cytosolic components have clarified correlations between regulated nuclear transport and cellular function. More and more reports concerning signal transduction regulatory mechanisms have focused on the importance of nuclear transport, making it crucial to know which transcription factors or regulatory proteins are transported into or out of the nucleus upon stimulation (e.g. treatment with light or certain hormones).
In this review, current progress in understanding the effects of light and certain plant hormones—auxin, brassinosteroid, gibberellin, cytokinin, and abscisic acid (ABA)—on nucleocytoplasmic shuttling of regulatory proteins is reported. What is known about nucleocytoplasmic transport of regulatory proteins, and the possible involvement of nuclear transport cargo proteins, are summarized in Table 1 and illustrated in Fig. 2.
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Auxin sensitivity and possible roles of nuclear pore complex proteins |
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Auxin is involved in diverse physiological and developmental processes, such as embryogenesis, phyllotaxis, and various tropisms. Long-distance polar transport of auxin from source to target cells via transporters and the resulting formation of auxin gradient have been implicated in these various aspects of development (Cho et al., 2007). On a molecular level in the cell, auxin mediates these actions by modulating transcriptional regulation of genes that encode auxin-responsive proteins (Woodward and Bartel, 2005). Much of this transcriptional regulation involves ubiquitin-mediated proteolysis of the AUX/IAA family of transcriptional repressors. These proteins suppress the ARFs (Auxin Response Factors) in the absence of auxin, but when auxin stimulates the cell, AUX/IAA proteins are degraded by a ubiquitin-dependent pathway, which releases the transcriptional repression. TRANSPORT INHIBITOR RESPONSE 1 (TIR1), one of the F-box components of the E3 ubiquitin ligase complex SCFTIR/AFB, is the major player in AUX/IAA degradation. TIR1 is actually an auxin receptor, and auxin binding to TIR activates SCFTIR/AFB (Dharmasiri et al., 2005; Kepinski and Leyser, 2005).
As signal transduction regulatory components acting in the nucleus, AUX/IAAs, ARFs, and TIR1 must be transported into the nucleus. Understanding how this particular process is regulated is emerging as another interesting line of study. Several reports document instances in which nucleocytoplasmic partitioning of proteins may participate in the regulation of auxin signalling. Recently, Parry et al. (2006) demonstrated that the extragenic suppressors of axr1 (sar1 and sar3) were defective in genes encoding nucleoporins (Nup160 and Nup96, respectively; Fig. 1A), and sar1/sar3 double mutations exhibited reduced nuclear localization of the AXR1 and AXR3/IAA17 proteins. AXR1, a subunit of the ubiquitin-related RUB-activating complex (Parry and Estelle, 2004), mediates auxin-dependent degradation of the Aux/IAA transcriptional regulators in the nucleus, so axr1 mutants are auxin-resistant.
Another nuclear pore complex (NPC)-associated protein, TRANSLOCATED PROMOTER REGION (TPR), was identified in a screen for early-flowering plant genes on the background of the late-flowering Arabidopsis mutant plants, luminidependence-1 (ld-1) (Jacob et al., 2007). In animals, the TPR protein is associated with the inner filaments of the nuclear basket, and it is thought to serve as a scaffold for the assembly of transport machinery (Krull et al., 2004; Fig. 1A). AtTPR is required for nuclear export of mRNA, and it also influences auxin sensitivity, as demonstrated by its ability to rescue the SUPPRESSOR OF AUXIN RESISTANCE 3 (SAR3) mutant phenotype when ectopically expressed (Jacob et al., 2007). Loss-of-function AtTPR mutants have a similar phenotype to HASTY (encodes an exportin 5 homologue) and SAR3 mutants (Bollman et al., 2003; Parry et al., 2006; Jacob et al., 2007), suggesting that AtTPR, HASTY, and SAR3 may play related roles in the function of the nuclear pore.
Ran regulates nuclear protein and nucleic acid transport, spindle assembly, and nuclear membrane reassembly during mitosis in mammals and yeasts (Joseph, 2006). A group of proteins, collectively known as Ran-binding proteins (RanBPs), controls the GTP/GDP-bound states of Ran and couples the Ran cycle to cellular processes. An overlay assay using Ran as a probe revealed three Arabidopsis RanBPs (33, 45, and 85 kDa in size) that preferentially bound to and stabilized the GTP-bound form of Ran (Lee et al., 2007b). From these three candidate proteins, Arabidopsis Ran binding protein 1c (AtRanBP1c) was cloned by yeast-two-hybrid screening, and the corresponding antisense transgenic plants showed longer-rooted primary roots and retarded lateral root growth (Kim et al., 2001). Interestingly, auxin sensitivity in these plants was 1000-fold higher than wild-type. This result, together with the fact that AtRanBP1c co-activates RanGAPs, has led scientists to speculate that the perturbed nucleocytoplasmic transport of proteins involved in auxin-regulated gene expression and mitosis is what underlies root-specific hypersensitivity to auxin (Kim and Roux, 2003). However, no direct evidence supports this hypothesis. In a more recent study, rice and Arabidopsis plants that ectopically expressed wheat Ran also showed altered auxin sensitivity, meristem size, and mitotic indices similar to those seen in the antisense AtRanBP1c transgenic plants (Wang et al., 2006). Auxin responses are mediated by successful nuclear transport of signalling regulators and transcription factors. Two examples are PAS1 (PASTICCINO 1, or AtFKBP71), which is one of the FK506-binding proteins (FKBPs), and FAN (FKBP-associated NAC), which is a plant NAC transcription factor (Smyczynski et al., 2006). FKBPs are one of three protein families (the FKBP, cyclophilin, and parvulin families) that have peptidyl-prolyl cis-trans isomerase (PPIase) activity (Barik, 2006). In plant seedlings, PAS1 and FAN move into the cell nuclei in response to auxin application (Smyczynski et al., 2006). The pas1 plants, which are loss-of-function mutants, exhibit aberrant cell division in their aerial tissues and form disorganized tumour-like structures, and these responses are closely associated with changes in the plants' responses to auxin and cytokinin (Harrar et al., 2003). Therefore, it is probable that auxin-triggered nuclear transport of PAS1 closely correlates with regulation of cell division. Other than their roles in mediating hormone responses, some FKBPs, such as TWD1 (TWISTED DWARF 1), modulate auxin efflux activities (Bouchard et al., 2006) by directly interacting with the P-glycoprotein auxin transporters AtPGP1 and AtPGP19 (Geisler et al., 2003). Protein interactions that link steroid receptor-Hsp90-FKBP52 immunophilin heterocomplexes to cytoplasmic dynein are common to plant and animal cells (Harrell et al., 2002), and these interactions stimulate nuclear import of steroid receptor complexes (Galigniana et al., 2002).
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Brassinosteroid-regulated localization of BZR1/BES1 transcription factors |
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Brassinosteroids (BRs) are polyhydroxylated steroid hormones, and they play pivotal roles in a wide range of plant growth and developmental processes, such as cell division, elongation/expansion in stems and roots, photomorphogenesis, reproductive development, tolerance to various environmental stresses, and xylem differentiation during vascular development (Haubrick and Assmann, 2006). Animal steroid hormones include the sex hormones (oestrogens, androgens, and progestins) and the adrenal cortex hormones (glucocorticoids and mineralocorticoids). Interestingly, although the steroid hormone biosynthetic enzymes are well conserved in plants and animals, perception and signal transduction of these hormones differ greatly between plants and animals. In the animal system, most steroid hormones bind to cytoplasmic receptors, and these complexes are transported into the nucleus to stimulate gene expression (Beato et al., 1995). In the currently-accepted plant model, BRs bind directly to the extracellular domain of the membrane receptor kinase BRI1, activate its kinase activity, and promote cross-phosphorylation and heterodimerization with another cell surface kinase, BAK1 (Nam and Li, 2002). This event somehow keeps the negative repressor BIN2 from phosphorylating the BES1 and BZR1 transcription factors, which leads to degradation of BES1/BZR1 by the 26S proteasome complex (He et al., 2002). Recent work suggested that BIN2 itself was also degraded in a BR-dependent manner, and its depletion strongly correlated with the BR-induced reduction in BIN2 activity (Peng et al., 2008). BR-induced activation of the BRI1/BAK1 receptor complex leads to dephosphorylation of the positive regulators BES1/BZR1, possibly by either inhibiting BIN2 activity or activating BSU1 phosphatase activity. Dephosphorylated BZR1 or BES1 then accumulates in the nucleus and directly binds to BR-responsive promoter elements, which alters expression of the genes involved in BR-induced growth response and homeostasis (He et al., 2005; Yin et al., 2005; Gendron and Wang, 2007).
Yin et al. (2005) proposed that the BR signalling pathway might be similar to the metazoan Wnt signalling pathway. This model emphasizes the effect of BRs on turnover or accumulation of key proteins, namely BZR1/BES1, in the nucleus. An initial study demonstrated that BR-induced dephosphorylation led to the accumulation of BZR1 and BES1/BZR2 proteins in the nucleus (Wang et al., 2002; Yin et al., 2002). By contrast, Vert and Chory (2006) demonstrated that BES1 constitutively localizes to the nucleus, and that the nuclear BIN2 kinase controls its activity. Phosphorylation of BES1 by BIN2 blocks its binding to target promoters and its transcriptional activity, and thus rather than regulating the nuclear translocation and accumulation of BES1, BIN2 seems to act in the nucleus to regulate the genomic response to BRs by phosphorylating BES1 and blocking its binding to target promoters and its transcriptional activity. Nonetheless, recent studies of Arabidopsis and rice BZR1 homologues clearly confirm that BZR1 functions as a nucleocytoplasmic shuttling protein, and that BIN2 kinase induces the nuclear export of BZR1 by modulating its interaction with the 14-3-3 proteins (Bai et al., 2007; Gampala et al., 2007; Ryu et al., 2007).
14-3-3 proteins are highly conserved phosphoprotein-binding proteins whose interaction with a partner is influenced by the phosphorylation states of both the target and the 14-3-3 protein itself (Aitken, 2006). Arabidopsis has at least 12 different 14-3-3 isoforms, and their binding partners reflect their subcellular localizations. Interestingly, Arabidopsis (Gampala et al., 2007) and rice (Bai et al., 2007) BZR1 and BES1 homologues possess conserved 14-3-3 binding sites, and these sites are the primary target of BIN2-mediated phosphorylation. Mutations in the 14-3-3 binding site not only abolish 14-3-3 binding, but they also increase BZR1 nuclear localization (Gampala et al., 2007). Along the same lines, binding of rice BZR1 (OzBZR1) to 14-3-3 proteins reduces BZR1 nuclear localization and inhibits its function (Bai et al., 2007). Based on these results, it was proposed that phosphorylation-mediated 14-3-3-binding may regulate cytoplasmic retention of the BZR proteins, thus depleting active BZR1 protein from the nucleus (Gendron and Wang, 2007).
Because BIN2 phosphorylates and destabilizes BZR1, it acts as a negative regulator of BR signalling (He et al., 2002). Nuclear-localized BSU1 phosphatase potentially dephosphorylates the BES1 protein, and a semi-dominant BSU1 mutant, bsu1-1D, accumulates more dephosphorylated BES1 in their nuclei after BL treatment (Mora-Garcia et al., 2004). A recent study transiently co-expressed BZR1 with HA-tagged BIN2 or BSU1 in mesophyll protoplasts; upon BR treatment, BSU1 rapidly enhanced BZR1 nuclear localization, directly opposing the action of BIN2 (which exports BZR1 out of the nucleus) (Ryu et al., 2007).
Two putative phosphorylation domains in the BZR1 protein, Ser-173 and Thr-177, are critical for the interaction between BZR1 and 14-3-3, thus acting as important regulatory sites for BIN2-mediated nuclear export of BZR1. It is now clear that BIN2 and BSU1 mediate phosphorylation and dephosphorylation of BZR1/BES1. Once phosphorylated, these proteins are either degraded by the 26S proteasome, inhibited with respect to DNA binding and transcriptional activity, or excluded from the nucleus by 14-3-3. By contrast, dephosphorylated BZR1/BES1 proteins may accumulate in the nucleus, and are therefore more likely to bind (or else their binding affinity is enhanced) to the BZR1/BES1-binding cis motif, which facilitates transcription of the target genes. What is not clear at this point is how this nucleocytoplasmic shuttling is regulated in the NPC, in concert with BR-dependent events occurring inside the nucleus. More information is needed to determine whether BR actually regulates the activity of any of the nuclear transport machinery components.
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Nuclear localization and gibberellin-regulated degradation of DELLA proteins |
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Gibberellins (GAs) are tetracyclic, diterpenoid phytohomones that are critically involved in regulating stem elongation, phase transition, floral initiation, sex determination, and germination (Ueguchi-Tanaka et al., 2007). Studying mutants impaired in GA response (GA-insensitive or hypersensitive mutants) has revealed that three components play important roles in GA signalling regulation: GA receptors, the DELLA family of repressor proteins, and F-box proteins (Zentella et al., 2007). In the absence of GA signalling in rice, the SLR1 (SLENDER RICE 1) DELLA-domain repressor blocks the transcription of GA-inducible genes, perhaps by binding and blocking the activity of a transcriptional activator. GA binds to the GID1 (GA-INSENSITIVE DWARF 1) receptor in the nucleus, and this GA-GID1 complex interacts with the DELLA repressor protein SLR1. The GA-GID1 complex then recruits an F-box protein, GID2 (GA-INSENSITIVE DWARF 2) of the SCFGID2 ubiquitin ligase complex, to mediate degradation of SLR1 by the 26S proteasome, releasing the transcriptional activator and allowing transcription to proceed (Hirano et al., 2008; Ueguchi-Tanaka et al., 2007).
DELLA domain-containing transcription factors, such as Arabidopsis GAI and RGA and rice SLR1, are intimately involved with nucleocytoplasmic transport or retention of proteins in response to GA signal transduction. Structurally, DELLA proteins have polymeric Ser and Thr regions, Leucine heptad repeats, and NLSs (Silverstone et al., 2001; Itoh et al., 2002), classic characteristics of nuclear proteins. Nuclear localization of both RGA and SLR1 has been demonstrated using GFP-tagged transgenic plants. After GA treatment, these two proteins rapidly disappear from the nucleus (Silverstone et al., 2001; Itoh et al., 2002). The phosphorylated form of SLR1 strongly accumulates in the nucleus in a gid2 background, while the same protein is ubiquitinated and degraded in the wild-type background (Sasaki et al., 2003; Gomi et al., 2004). Despite accumulating evidence, it is currently not clear how these F-box and GID1 proteins are transported into and reconstituted in the nucleus in order to drive GA-dependent degradation of the DELLA repressors. Therefore, it is critical that future studies address whether GA regulates this nuclear import process and whether any possible GA-dependent molecular events occur in nucleoporins assembled at the NPCs.
Besides repressing GA signalling, DELLA proteins also co-ordinately modulate other hormone, light, and stress signalling pathways. For example, RGA directly interacts with the phytochrome-interacting proteins PIF3 (Feng et al., 2008) and PIF4 (Lucas et al., 2008), thereby blocking their transcriptional activities. DELLA proteins might also integrate the growth-promoting effects of the ethylene, auxin, and GA signalling pathways (Achard et al., 2003), in order to respond to environmental cues from adverse conditions, such as high salinity (Achard et al., 2006).
In potatoes, GA stimulates nuclear import of PHOTOPERIOD RESPONSIVE 1 (PHOR1), which shows significant homology to Drosophila Armadillo and is involved in tuberization (Amador et al., 2001). PHOR1 is an ubiquitin E3 ligase that promotes GA responses; therefore, PHOR1 acts as a positive regulator in GA signalling (Monte et al., 2003). Currently, the target of PHOR1 E3 ligase is not known. PHOR1 has seven Arm-repeat domains and an N-terminal CPI (Cys-Pro-Ile) domain, and its nuclear import requires the Arm repeat domains. PHOR1 might also participate in regulating GA responses, because PHOR1 antisense transgenic plants were dwarfed and less sensitive to GA than wild-type plants (Amador et al., 2001), and because PHOR1-overexpressing transgenic plants exhibit the opposite phenotypes. It would be now interesting to know whether the PHOR1 protein is transported into the nucleus in a GA-dependent manner, and how it is subsequently involved in DELLA degradation. Moreover, because PHOR1 is also photoperiod responsive, this protein is an appealing candidate as a cross-talk point between the light and GA signal transduction pathways.
Plants can detect changes in their endogenous GA levels and accordingly modulate their developmental programs (Lee and Soh, 2007). RSG (REPRESSION OF SHOOT GROWTH) is a transcriptional activator that has a basic leucine zipper domain, and it regulates endogenous GA levels (Fukazawa et al., 2000). GA affects the nuclear localization of the RSG protein in tobacco (Ishida et al., 2004). Similar to the BR signal transduction pathway, 14-3-3 proteins suppress RSG by sequestering it in the cytoplasm (Igarashi et al., 2001). This process depends on phosphorylation of RGS (Ishida et al., 2004). A mutant form of RSG that does not bind to 14-3-3 is predominantly localized in the nucleus and shows higher transcriptional activity than the wild-type protein (Igarashi et al., 2001). Based on these results, the authors proposed that endogenous GA levels regulate intracellular localization of RSG by modulating 14-3-3 binding, in order to maintain GA homeostasis. In brief, RSG's dissociation from 14-3-3 in response to a drop in GA levels promotes nuclear accumulation of RSG. A spike in GA levels causes cytoplasmic migration of RSG through phosphorylation of RSG and 14-3-3 binding.
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Hormone-dependent nuclear localization of regulatory proteins in cytokinin and ABA signal transduction |
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Cytokinins are synthesized from adenine and influence diverse physiological and developmental processes: cell division, stem cell control of shoot and root development, vascular differentiation, leaf senescence, and stress tolerance (Mok and Mok, 2001). Cytokinin signal transduction uses a multi-step two-component phospho-relay system: (i) hybrid histidine protein kinases (AHKs) mediate sensing and signalling initiation; (ii) histidine phosphotransfer proteins (AHPs) relay the phosphates and promote nuclear import of AHPs; (iii) phosphates are transferred from the AHPs to B-type nuclear response factors (ARRs) that activate transcription; (iv) B-type ARRs negatively regulate the A-type ARRs using feedback control (Müller and Sheen, 2007).
The key event here is the nuclear import of AHPs. By tracking GFP-fused AHP1 and AHP2 in vivo, Hwang and Sheen (2001) demonstrated that these regulatory proteins are imported to the nucleus in a cytokinin-dependent manner. In the nucleus, AHP1 and AHP2 transfer phosphates to ARR1, ARR2, and ARR10, which activates these proteins to act as transcriptional activators of cytokinin-inducible ARR4, ARR5, ARR6, and ARR7. Even though some in vivo evidence supports the nuclear import of AHP1 and AHP2, no reports thus far have elucidated the regulatory mechanism behind this transport process.
In contrast to the unknown nuclear transport mechanism in cytokinin signalling, several reports have unravelled how ABA signalling regulates cargo transport. One study obtained an ABA hypersensitive mutant, sad2 (super sensitive to ABA and drought 2), by screening a T-DNA mutagenized population of RD29A:LUC plants. This mutant exhibits increased luciferase activity after ABA, salt, cold, or polyethylene glycol treatment (Verslues et al., 2006). The study found that SAD2 encoded an importin β-domain family protein; this result, together with its localization to the nuclear periphery, led the authors to propose that SAD2 might be involved in the nuclear import of a negative ABA regulator (or nuclear export of a positive regulator) (Verslues et al., 2006). In addition, SAD2 also mediates the nuclear transport of MYB4, a protein required for UV-B responses (Zhao et al., 2007). Another ABA hypersensitive mutant, abh1 (abscisic acid hypersensitive 1), lacks a functional mRNA cap-binding protein that might be involved in nuclear RNA processing and export through the NPC (Bezerra et al., 2004).
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Effects of light: phytochrome-, chryptochrome-, and UV-B-mediated nuclear localizations of downstream effectors |
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Light is one of the most important environmental factors required for plant growth and development. Applying a relatively dim light to a dark-grown seedling induces dramatic shifts in its transcriptome patterns within hours, quickly mediating downstream developmental changes (photomorphogenesis). These changes include up-regulation of genes that synthesize photosynthetic machinery, as well as a decrease in the rate of stem elongation, the beginning of apical-hook straightening, and the initiation of pigment synthesis (Casal and Yanovsky, 2005). Various and delicate photosensory molecules, namely phytochromes (red/far-red receptors), cryptochromes, the carotenoid zeaxanthin, and phototropins (blue light receptors), sense the intensity, quality, and direction of light. While no one has identified a UV-B-specific photoreceptor, it is clear that a photomorphogenic UV-B signal (low fluence rates of UV-B) stimulates expression of a wide range of genes, including those involved in DNA repair and oxidative stress management. These responses protect plants from the oxidative UV-B damage inevitably caused by sunlight (Ulm et al., 2004; Jenkins and Brown, 2007).
Light-regulated nuclear transport of phytochromes and cryptochromes
Phytochromes form homo- or heterodimers in the cell, and they exist in two spectrophotometrically different, but photoconvertible forms (Jones and Edgerton, 1994): the red light-absorbing form (Pr; 
max=667 nm), and the far-red light absorbing form (Pfr; max=720 nm) (Quail et al., 1995). Pfr is the physiologically active form in most photomorphogenic responses. Arabidopsis plants harbour five different phytochrome genes (PHYA to PHYE) (Clack et al., 1994) that are divided into two types according to their light stability. PHYA is the only photo-labile type I phytochrome in Arabidopsis. PHYB to PHYE are all type II phytochromes and are relatively stable in light (Franklin and Whitelam, 2004).
Light-regulated gene expression is controlled at different levels: transport of photoreceptors into the nucleus, turnover of photoreceptors, transcriptional control by several transcription factors, proteolysis of transcription factors, and protein–protein interaction with photoreceptors, either with other photoreceptors or with transcription factors (Lorrain et al., 2006; Han et al., 2007). During phytochrome signal transduction, plants use phosphorylation-dependent signal relay machinery that resembles a bacterial two-component system; thus, phytochromes of higher plants can act as auto-regulatory, light-inducible sensing, serine/threonine protein kinases by using their light-absorbing phytochromobilin chromophores (Sharma, 2001). Upon light absorption, the inactive Pr undergoes a conformational change that exposes its C-terminal region, the region involved in nuclear transport and nuclear body (NB) formation, to promote selective movement of the active Pfr into the nucleus (Chen et al., 2005b). Although the C-terminal half of PHYB contains signals for both nuclear import and nuclear body (NB) localization, primary sequence analysis has not identified a conventional NLS (Chen et al., 2005b).
Importantly, while all phytochromes are transported into the nucleus upon white and red light treatment (Kircher et al., 2002), each phytochrome exhibits different light quality requirements and import kinetics (Kircher et al., 2002; Nagy and Schäfer, 2002). PhyA transport is rapid (15 min after irradiation), and blue, red, and far-red light promote its transport (Kircher et al., 2002). Light-dependent nuclear localization of physiologically-active phyA (i.e. in Pfr form) is regulated through its interaction with plant-specific FHY1 (Far-red Elongated Hypocotyls 1) and FHL (FHY1-like) (Hiltbrunner et al., 2005, 2006). Recent reports demonstrated that two transposase-derived transcription factors, FHY3 and FAR1 (Far-red Impaired Response 1), directly bind to an FBS motif (CACGCGC in sequence) in the promoter of FHY1 and FHL genes, and these transcription factors activate gene expression to promote phyA nuclear accumulation. (Lin et al., 2007). In contrast to phyA, phyB exhibits slower transport kinetics, and only in response to red light (Kircher et al., 2002). Nuclear import of phyB occurs in the manner of LF (low fluence) of phytochrome, and it shows R/FR reversibility and saturability (Nagy and Schäfer, 2002; Chen et al., 2005b). This differential regulation of phytochrome transport may confer functional specificity. After the phytochromes are imported, speckles (i.e. NBs) form in the nucleus (Kircher et al., 2002). Although the nature of these NBs is still hazy, they must be complexes of the phytochromes and their binding proteins: these binding proteins colocalize with the phytochrome after irradiation, and speckle formation coincides with the onset of phytochrome functionality (Kircher et al., 2002). Inside the nucleus, the phytochrome interacts with nuclear regulatory proteins, such as phytochrome interacting factors (PIFs, Castillon et al., 2007), COP1 (Seo et al., 2003), and cry2 (Mas et al., 2000), ultimately leading to changes in plant growth and development. Recent work has revealed that light-activated phytochrome is transported into the nucleus, binds to PIF3, and forms NBs. After that, PIF3 is phosphorylated and degraded (Al-Sady et al., 2006).
Other well-known classes of photoreceptors are the cryptochromes (CRY) and the phototropins (such as PHOT1 and PHOT2). They all absorb blue/UV light. However, CRY proteins are present both in the cytoplasm and in the nucleus, while PHOT proteins are plasma membrane-localized receptor kinases (Sakamoto and Briggs, 2002). Since they are nuclear proteins, our discussion herein will be limited to cryptochromes.
Cryptochromes mediate several photomorphogenetic responses, such as inhibition of hypocotyl elongation, cotyledon expansion and opening, and induction of anthocyanin accumulation (Lin and Shalitin, 2003). The first cryptochrome to be identified was Arabidopsis AtCRY1 (Ahmad and Cashmore, 1993), after which other studies identified AtCRY2 and other orthologues from various organisms. The N-termini of the CRY proteins contain a flavin chromophore-binding photolyase-like domain; however, these proteins do not exhibit photolyase activity (Lin and Todo, 2005).
The subcellular localization of cryptochromes differs depending on light conditions and the species (Table 2). For example, Arabidopsis CRY1 is nuclear-localized in the dark but localizes to the cytoplasm under white light, while Arabidopsis CRY2 is largely nuclear under both dark and light conditions (Yang et al., 2000; Guo et al., 1999). Another recent study reveals that nuclear and cytoplasmic CRY1 perform separate functions during blue light-induced photomorphogenesis; for example, nuclear CRY1 effectively mediated light-induced inhibition of hypocotyl or stem elongation, whereas the cytoplasmic pool of CRY1 proteins did not. Conversely, cytoplasmic CRY1 promoted primary root growth and cotyledon expansion in blue light, while nuclear CRY1 inhibited these responses (Wu and Spalding, 2007). As nuclear CRY2 mediates blue light-induced inhibition of hypocotyl elongation, it is concomitantly ubiquitinated and degraded in a phosphorylation- and 26S proteasome-dependent manner in the nucleus in response to relatively high-intensity blue light irradiation (Yu et al., 2007). The authors proposed that these multiple thresholds of CRY2 phosphorylation in response to different blue light intensities may serve as an adaptive response that enables plants to respond differentially to the ever-changing light environment in nature.
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In the case of a fern, Adiantum capillus-veneris, five genes encode cryptochromes (Imaizumi et al., 2000). As in Arabidopsis, all Adiantum cryptochromes show unique localization and light response patterns. Adiantum CRY3 and CRY4 localize to the gematophyte nucleus, and the nuclear localization of Adiantum CRY3 is regulated by light (Imaizumi et al., 2000). This difference might be due to dissimilarity in their C-terminal amino acid sequences. The rice CRY1 orthologue has two nuclear localization domains, but the protein is present in the nucleus and the cytoplasm (Matsumoto et al., 2003). Once in the nucleus, CRY1 and CRY2 are independently involved in regulating early gene expression in the blue light signal transduction pathway (Ohgishi et al., 2004).
UV-B-induced UVR8 nuclear localization and SAD2-mediated UV-B responses
UV-B light (280–320 nm) is a stress factor in plants; specifically, high fluence UV-B light inhibits photosynthesis, induces stress responses, damages DNA and other molecules, and in some cases causes necrosis (Jenkins and Brown, 2007). However, low-fluence rates of UV-B light can act as informational signals that direct expression of a wide range of genes, thus regulating plant growth and development (Brown et al., 2005; Brown and Jenkins, 2007). To understand further how plants defend themselves against the harmful effects of UV light, one group isolated and characterized an Arabidopsis UV-B-hypersensitive mutant uvr8-1 (UV resistance locus 8-1) (Kliebenstein et al., 2002). The uvr8 mutant is not able to induce chalcone synthase gene expression, and DNA microarray analysis using uvr8 and hy5 mutants revealed that UVR8-regulated gene expression protects plants from UV and DNA damage (Ulm et al., 2004; Brown et al., 2005). In chromatin immunoprecipitation experiments, UVR8 associated with the HY5 promoter region and regulated its expression, using it as a key effecter in the UV-B-specific UVR pathway (Brown et al., 2005).
UVR8 is structurally similar to human RCC1, the protein that exchanges GDP for GTP in the nuclear small GTP binding protein Ran (Kliebenstein et al., 2002). However, UVR8 does not exhibit nucleotide exchange activity; instead, it binds to histones in the chromatin (Brown et al., 2005). Of particular interest, UV-B promotes rapid nuclear localization of UVR8, probably by promoting active translocation of a fraction of the cytoplasmic UVR8 pool, and this nuclear accumulation leads to UV-B-mediated induction of the HY5 gene (Kaiserli and Jenkins, 2007). Although this experiment yielded very little information on the mechanism of this nuclear localization, the authors speculated that the N-terminal region of the UVR8 protein may bind to proteins that facilitate nuclear import, specifically in response to UV-B. Interestingly, both COP1 and HY5 accumulate in the nucleus after UV-B light treatment, and COP1 acts as a positive regulator in UV-B signal transduction. This function is diametrically opposed to its role in phytochrome signal transduction (Oravecz et al., 2006).
Another defective UV-B response mutant, sad2, lacks a functional importin β-like protein and is hypersensitive to ABA treatment (Verslues et al., 2006). Following UV-B irradiation, sad2 also shows more tolerance and less DNA damage than wild-type plants. Levels of the MYB4 transcriptional repressor and cinnamate 4-hydroxylase (C4H), a key enzyme that produces UV-absorbing compounds, are significantly higher in sad2 than in wild-type plants (Zhao et al., 2007). MYB4 is a negative regulator of C4H transcription and of its own transcription. Because nuclear accumulation of MYB4 was absent in the sad2 mutant, the authors proposed that this mutant exhibited an altered negative autoregulatory MYB4 feedback loop, resulting in constitutive expression of MYB4 and C4H, which gave the mutant a higher tolerance to UV-B light. This example clearly demonstrates that a general nuclear import component like SAD2 can affect several cellular signalling pathways and their downstream physiological responses.
Light-regulated nuclear transport of transcription factors and COP1-regulated protein degradation
Tightly-controlled nuclear import of transcription factors and other proteins involved in proteolysis is one of the regulatory mechanisms by which plants transfer light signals from the cytoplasm to the nucleus. One example is the parsley CPRF bZIP proteins. CPRF1 localizes to the nucleus, CPRF2 to the cytosol, and CPRF4 to both compartments. CPRF2 is imported to the nucleus upon light treatment (Kircher et al., 1999; Harter et al., 1994), and the high-irradiance response (HIR) by phyA and the low-fluence response by phyB are both involved in this translocation (Kircher et al., 1999). Light also regulates nucleocytoplasmic localization of Arabidopsis G-box-binding proteins (GBFs): Histochemical localization and cellular fractionation studies of GUS-GBF fusion proteins in a soybean cell culture system demonstrated that under all light conditions tested, GBF1 localized to the cytoplasm while GBF4 was nuclear (Terzaghi et al., 1997). Moreover, GBF2 exhibited blue light-dependent translocation from the cytoplasm to the nucleus (Terzaghi et al., 1997).
COP1, a RING-finger protein with seven WD-40 repeats and a coiled-coil domain, acts as a negative regulator of photomorphogenesis (Yi and Deng, 2005). COP1 has nuclear import and export signal sequences, and its nuclear localization is reciprocal to that of phytochromes; i.e. it is in the nucleus in the dark and is exported to the cytoplasm after light treatment (Stacey et al., 1999; Subramanian et al., 2004). As an E3 ubiquitin ligase, COP1 adds ubiquitin tags to induce degradation of target proteins in the light signal transduction pathway (Jang et al., 2005; Yi and Deng, 2005).
Nuclear Arabidopsis COP1 interacts with many downstream targets through its WD-40 domain, promotes their degradation by tagging them with ubiquitin, and thus represses photomorphogenesis in the dark. These targets include transcription factors that positively regulate photomorphogenesis in the light, such as HY5 (Osterlund et al., 1999), HYH (Holm et al., 2002), LAF1 (Seo et al., 2003), PIF3 (Bauer et al., 2004), and HFR1 (Jang et al., 2005; Yang et al., 2005). COP1 also targets light-labile phyA (Seo et al., 2004), CRY1, and CRY2 (Shalitin et al., 2002; Sang et al., 2005), so COP1 may also prevent hyperactivation of light-induced photomorphogenesis. Therefore, one way of controlling COP1 activity is to perform light-dependent nuclear-cytoplasmic repartitioning to exclude the protein from the nucleus.
In Arabidopsis, the nuclear-localized suppressor of phyA-105 (SPA1) protein, which is structurally related to COP1 in its coiled-coil and carboxyl WD-repeat domains, is an integral component of the COP1-SPA1 E3 ubiquitin ligase complex. This complex mediates targeted degradation of HY5 and HFR1 (Yang and Wang, 2006). The authors proposed that SPA1 may enhance COP1's substrate binding activity or ubiquitination efficiency. Alternatively, SPA1 may promote nuclear accumulation of COP1, thus prolonging its repressive activity. It would be interesting to test whether SPA1 localization is also influenced by light treatment.
By performing an in vitro binding assay using a native gel electrophoresis, Jiang et al. (2001) demonstrated that an importin isoform in rice, importin 1b, together with importin β, preferentially bound to the conserved NLS to form a stable pore-targeting complex (PTAC) and dock at the nuclear rim of digitonin-permeabilized HeLa cells. Addition of mouse Ran-GDP efficiently translocated the docking complex into the nucleus. COP1 is predicted to have putative monopartite- and bipartite-type NLS sequences. Interestingly, only the bipartite-type NLS is a functional NLS, and mutations in this domain abolish nuclear localization, in onion epidermal cells or in roots of an NLS-GFP transgenic Arabidopsis (Jiang et al., 2001).
Recently, a nuclear trafficking assay utilized a virus-induced gene silencing (VIGS) system to knock down importin homologues has proved to be a powerful technique to study the mechanisms underlying protein transport from the cytoplasm to the nucleus in plants (Kanneganti et al., 2007). In this system, reconstitution of known plant nucleoporins, Ran-GDP/Ran-GTP, and Ran-binding proteins, and transiently testing the resulting effect on nuclear accumulation of GFP-fused COP1, would provide useful information concerning which proteins are important in regulating nuclear import and export of COP1 (and whether their involvement is light-regulated).
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Possible involvement of sumoylation and O-GlcNAc modification in nucleocytoplasmic regulation in plants |
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In animals and yeast, post-translational SUMOylation and O-linked β-N-acetylglucosamine (O-GlcNAc) modification of nucleocytoplasmic proteins can efficiently regulate stimulus-dependent nucleocytoplasmic transport and intranuclear protein targeting (Love and Hanover, 2005; Andrali et al., 2007; Meulmeester and Melchior, 2008). In plants, many NPC and nuclear proteins are either SUMOylated or O-GlcNAc modified (Heese-Peck et al., 1995; Saracco et al., 2007). The SUMO proteins (AtSUMO1/2), a SUMO E2 conjugation enzyme (AtSCE1), a SUMO E3 ligase (AtSIZ1), a SUMO protease (AtULP1), and an O-GlcNAc transferase (OGT) that participate in this process have been identified and characterized (Miura et al., 2007b; Silverstone et al., 2007).
In mammals, SUMOylation of target proteins regulates diverse cellular processes, most notably transcriptional repression and maintenance of chromosomal integrity (Geiss-Friedlander and Melchoir, 2007). In terms of nucleocytoplasmic transport, SUMOylation can alter the subcellular localization of the target protein by altering its protein–protein interactions. In mammals, SUMOylated RanGAP1 localizes to the nuclear pore by interacting with the nucleoporin RanBP2 protein, whereas unmodified RanGAP1 remains cytosolic (Mahajan et al, 1997). By contrast, anchoring plant RanGAP to the nuclear envelope does not require SUMOylation; instead, it requires an N-terminal plant-specific WPP domain (Jeong et al., 2005) and the corresponding Arabidopsis WPP-domain interacting proteins (WIPs, Xu et al., 2007). Nonetheless, the Arabidopsis SUMO proteins (AtSUMO1/2) interact with a SUMO-conjugating E2 enzyme orthologue (AtSCE1a), and AtSCE1a was able to conjugate human SUMO1 to human RanGAP1 in vitro (Lois et al., 2003). Balance between an isopeptidase that removes SUMO and a SUMO E3 ligase that adds SUMO at the nuclear pore complexes of certain targets is coupled to their shuttling into and out of the nucleus (Pichler and Melchior, 2002). Accumulating evidence suggests that nucleocytoplasmic regulation and SUMOylation are interdependent processes that both strongly influence nucleocytoplasmic transport (Pichler and Melchior, 2002). Interestingly, transiently-expressed AtSUMOs and AtSCE1a co-localized at the nucleus or in nuclear bodies in epidermal onion cells. Moreover, transgenic plants with AtSCE1a co-suppression showed hypersensitive root growth inhibition in response to ABA treatment, but increased SUMOylation levels attenuated this ABA-mediated growth inhibition (Lois et al., 2003). Recent reports detailed other regulatory roles of SUMOylation in plants such as: the SUMO E3 ligase AtSIZ1 induces SUMOylation in salicylic acid-mediated innate immunity (Lee et al., 2007a), AtSIZ1-mediated ICE1 SUMOylation regulates freezing tolerance (Miura et al., 2007a), and stress induces SUMOylation of nuclear proteins, as detected by SUMO1-specific antibodies (Saracco et al., 2007).
Either O-GlcNAc glycosylation or phosphorylation close to the NLS of the viral Jun protein almost completely excluded it from the nuclei of mouse NIH/3T3 cells (Schlummer et al., 2006). By comparison, high glucose conditions promoted the association of the NeuroD1 transcription activator with OGT in mouse MIN6 cells, and the resulting O-GlcNAc modification of the protein enhanced its nuclear localization, which activated insulin gene expression (Andrali et al., 2007). Arabidopsis SPINDLY (SPY) and SECRET AGENT (SEC) are putative plant OGTs; they either glycosylate the capsid protein of the Plum poxvirus (SEC, Chen et al., 2005a) to influence viral movement, or they negatively regulate GA signalling by O-GlcNAcylating RGA or GAI DELLA proteins (Silverstone et al., 2007). Interestingly, O-GlcNAc modification of DELLA repressors, such as RGA, may stimulate their activity without affecting their nuclear localization (Silverstone et al., 2007). Other than this single report, there are no data that implicate O-GLcNAc modification in the regulation of nucleocytoplasmic transport.
In terms of selective and non-selective macromolecular trafficking, cell-to-cell movement of endogenous and viral non-cell-autonomous proteins (NCAPs) through the plasmodesmata, and long-distance movements of NCAPs through the phloem, show interesting structural and functional parallels with protein transport through the nuclear pore complex (Lee et al., 2000). A phosphorylation/O-GlcNAc recognition motif controls the binding of a specific subset of phloem NCAPs to NCAPP1 (Non-Cell-Autonomous pathway Protein 1) and subsequently regulates their transport through the plasmodesmata (Taoka et al., 2007). It would be worthwhile to compare the nuclear proteomes of SUMO or OGT knock-out mutants with wild-type plants, in order to identify whether a pool of nuclear/cytoplasmic proteins is SUMOylated or O-GlcNAcylated.
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Concluding remarks and perspectives |
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The correct signal-dependent reconstitution of transport machinery, together with its subsequent regulation of nuclear import and export of proteins and RNAs, is crucial in order for cells to exchange intrinsic and intracellular information. Furthermore, whether proteins and RNAs are in the right place at the right time is a critical factor in normal development. To understand hormone- and light-induced regulation of nucleocytoplasmic transport of key players and to understand generalities in how these processes are regulated, recent advances in these fields have been reviewed, and the possible implications of nucleoporins and other transport-regulating proteins, such as Ran small G-protein and its binding proteins have been discussed.
There are several ways in which light- or hormone-induced nucleocytoplasmic localization of regulatory proteins could contribute to the corresponding signalling pathways (summarized in Table 3; Fig. 2). One way is to drive or accumulate positive modulators in the nucleus and to direct the proteolytic degradation of their repressor proteins. This regulation leads to de-repression of the stimulus-responsive transcription factors and promotes gene expression. In the presence of hormones or light stimulus, these processes rely on the SCF complex, which modifies the target proteins with ubiquitin and triggers their proteolytic degradation via the 26S proteasome. Many signalling pathways use this regulatory mode, as seen in TIR1-induced degradation of AUX/IAAs and GID2- or PHOR1-induced degradation of DELLA proteins.
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Phosphorylation/dephosphorylation events can also play important roles in regulating protein degradation and exclusion from the nucleus. BIN2-phosphorylated BZR1, for example, is either destined for proteolytic degradation, or it is excluded from the nucleus under the guidance of 14-3-3 proteins. BSU1 phosphatase reverses this process, leading to nuclear accumulation of dephosphorylated BZR1. Active GAs cause cytoplasmic migration of RSG by enhancing its phosphorylation and binding to 14-3-3.
In the case of light signalling, the COP1 E3 ligase shuttles in and out of the nucleus, depending on specific light conditions, which affects the life and death of light-regulated transcription factors like HY5, the PIFs, and even the phytochrome itself. Photoreceptors themselves are transported into the nucleus in a light-dependent manner, and their turnover is tightly regulated by other mechanisms, such as binding to the light-related proteins and kinases. In addition to the regulatory proteins mentioned above, many nuclear proteins are also imported into or exported out of the nucleus in a stimulus-dependent manner, as seen in the auxin-induced nuclear movement of PAS1 and FAN, the cytokinin-driven nuclear localization of AHP1 and AHP2, the light-dependent nuclear transport of CPRF2 and GBFs, and UV-B-induced UVR8 nuclear localization.
The importance of nuclear transport machinery in regulating plant growth and development is evidenced by the many hormone-insensitive or -hypersensitive mutants that are defective in components or factors regulating nuclear transport, such as proteins in the NPC, Ran, or the RanBPs. SAR1 and SAR3 (which are extragenic suppressors of auxin resistant axr1 or axr3) are nucleoporins, and ectopic expression of NPC-associated AtTPR in a sar3 mutant background rescues its auxin phenotype. Mutations in AtTPR and SAR3 show an auxin phenotype that resembles the loss-of-function mutation in HASTY (which encodes exportin 5). Ectopic expression of the small GTP-binding Ran1 and antisense expression of Ran-binding AtRanBP1c cause auxin hypersensitivity. A mutation in the SAD2 gene, encoding a protein with an importin β domain, not only alters the plants' sensitivity to ABA and drought but also to UV-B. Rice importin 1b, together with importin β, preferentially binds to a bipartite NLS of COP1 and facilitates its nuclear localization. In addition, nucleocytoplasmic trafficking regulated by the NPC/Ran/RanBPs transport-regulating machinery in plants is reportedly involved in many other cellular processes, including temperature signalling, plant–pathogen interactions, nuclear export of small RNAs, and regulation of nuclear Ca2+ influx (Meier, 2005).
Increasing evidence supports critical roles for stimulus-induced nuclear localization of regulatory proteins; these reports indicate that nucleocytoplasmic shuttling of proteins could be one of the most basic regulatory mechanisms in plants. However, currently, reports do not adequately reveal how certain hormones regulate the nuclear transport of specific proteins, nor do they address what transmits the information from the hormone action to the downstream nuclear transport events. In other words, it remains to be discovered whether mutations affecting nuclear transport-regulating components in various signalling pathways are indeed regulatory, or whether they are non-specific, indirect outcomes of other effects. Therefore, it will be necessary to find the hormone-specific factor(s)/modifications that regulate nucleocytoplasmic transport and to understand the stimulus-dependent events that occur at the NPC. What factor(s)/modification(s) is (are) involved in activating nuclear transport of SCF or transcription factors after hormone entry? Is the regulation of nuclear transport by diverse nucleoporins selective, or is it a general response to diverse light and hormone signalling pathways? These questions highlight promising areas to be explored in the future.
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Acknowledgements |
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We thank Thomas Bushart and Dr Stanley J Roux at The University of Texas at Austin, USA for their critical reading and thoughtful comments on the manuscript. This work was supported by Korea Research Foundation Grants funded by the Korean Government, Basic Research Promotion Fund (KRF-2007-313-C00687 and KRF-2006-311-C00149).
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